Mobile brain/body imaging of landmark‐based navigation with high‐density EEG

• Published in: The European journal of neuroscience 2021-12, Vol.54 (12), p.8256-8282
• Main Authors: Delaux, Alexandre, Saint Aubert, Jean‐Baptiste, Ramanoël, Stephen, Bécu, Marcia, Gehrke, Lukas, Klug, Marius, Chavarriaga, Ricardo, Sahel, José‐Alain, Gramann, Klaus, Arleo, Angelo, Solis‐Escalante, Teodoro
• Format: Article
• Language: English
• Subjects: Brain - diagnostic imaging; Brain mapping; Brain Waves; Coding; Cognitive ability; Cognitive science; Computer applications; ecological navigation; EEG; Electroencephalography; Functional magnetic resonance imaging; Humans; Information processing; Magnetic Resonance Imaging - methods; Medical imaging; mobile EEG; Navigation behavior; Neuroimaging; Neuroscience; Proprioception; retrosplenial complex; Sensorimotor system; Sensory integration; source reconstruction; Spatial discrimination learning; Spatial Navigation; Special Issue; Synchronization; virtual reality; Young Adult; Young adults
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.15190

Coupling behavioral measures and brain imaging in naturalistic, ecological conditions is key to comprehend the neural bases of spatial navigation. This highly integrative function encompasses sensorimotor, cognitive, and executive processes that jointly mediate active exploration and spatial learning. However, most neuroimaging approaches in humans are based on static, motion‐constrained paradigms and they do not account for all these processes, in particular multisensory integration. Following the Mobile Brain/Body Imaging approach, we aimed to explore the cortical correlates of landmark‐based navigation in actively behaving young adults, solving a Y‐maze task in immersive virtual reality. EEG analysis identified a set of brain areas matching state‐of‐the‐art brain imaging literature of landmark‐based navigation. Spatial behavior in mobile conditions additionally involved sensorimotor areas related to motor execution and proprioception usually overlooked in static fMRI paradigms. Expectedly, we located a cortical source in or near the posterior cingulate, in line with the engagement of the retrosplenial complex in spatial reorientation. Consistent with its role in visuo‐spatial processing and coding, we observed an alpha‐power desynchronization while participants gathered visual information. We also hypothesized behavior‐dependent modulations of the cortical signal during navigation. Despite finding few differences between the encoding and retrieval phases of the task, we identified transient time–frequency patterns attributed, for instance, to attentional demand, as reflected in the alpha/gamma range, or memory workload in the delta/theta range. We confirmed that combining mobile high‐density EEG and biometric measures can help unravel the brain structures and the neural modulations subtending ecological landmark‐based navigation. Despite the inherent mobility of natural navigation, there is only a handful of recordings of human brain activity during active exploration in space. Using Mobile Brain/Body Imaging on subjects performing landmark‐based reorientation, we retrieved exploitable neural signals in deep cortical regions and a set of visual, somatosensory, and motor areas. We discuss their neurobehavioral dynamics with respect to similar static experimental paradigms and mobile EEG correlates of locomotion control.